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The Immunobiology of <Emphasis Type="Italic">Acanthamoeba

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The Immunobiology of <Emphasis Type= Springer Semin Irnmunopathol (1999) 21 : 147-160 Springer Seminars in Immunopathology © Springer-Verlag 1999 The immunobiology of Acanthamoeba keratitis Jerry Y. Niederkorn, Hassan Alizadeh, Henry F. Leher, James P. McCulley Department of Ophthalmology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9057, USA Background Although only a few centimeters in diameter, the eye is composed of virtually every type of tissue found in the remainder of the body, as well as cellular and noncellular el- ements found nowhere else [37]. The eye is an extension of the brain, and, as such, conducts an enormous array of neurological functions. The million ganglion cells of the retina transmit 500 electrical signals per second, which in computer terms is equiv- alent to 1.5 × ]0 9 bits of information [37]. However, if the cornea loses transparency, complex functions of the retinal elements are rendered meaningless, and acute vision is preempted. To prevent this loss from happening, the eye utilizes anatomical, physi- ological, and immunological barriers to shield the cornea from injury and infection [43]. In many animals the eye is recessed in cranial sockets and surrounded by bony protuberances protecting it from blunt trauma. The eyelids and tear film serve as effective barriers against environmental agents, including air- and water-borne patho- gens. The cornea is exposed continuously to the external environment and potential patho- gens. One might expect any infectious agent encountered at the ocular surface would be met with a vigorous immune response that would promptly eliminate the pathogen and protect the cornea. However, in certain cases, a zealous immune response to corneal pathogens can have the opposite effect, contributing instead to loss of corneal transparency and blindness. Ironically, the three most common causes of infectious blindness - trachoma, herpes simplex virus (HSV) keratitis, and onchocerciasis - are immune-mediated diseases [43, 51, 65]. A recent study suggests the pathogenesis of one of the most common bacterial infections of the cornea, Pseudomonas aeruginosa keratitis, is also immune-mediated [26]. Thus, immune-mediated diseases of the cornea are not restricted to a specific category of pathogen, as the previous examples included a helminth (Onchocerca volvulus), a virus (HSV), an intracellular bacterium (Chlamydia trachomatis), and an extracellular bacterium (P. aeruginosa). With this Correspondence to: J. Y. Niederkom 148 J.Y. Niederkorn et al. information in mind, we suspected the pathogenesis of another corneal infection, Acanthamoeba keratitis, also might be immune-mediated. Acanthamoeba keratitis is a sight-threatening corneal disease caused by patho- genic, free-living amoebae [3-5]. At least eight species of Acanthamoeba have been implicated in corneal infections: A. castellanii, A. culbertsoni, A. polyphaga, A. hatch- etti, A. fhysodes, A. lugdunesis, A. quina, and A. griffini [59]. Acanthamoeba spp. are ubiquitous organisms that can be isolated from a wide range of environmental sites, in- cluding fresh water reservoirs, salt water, swimming pools, hot tubs, ventilation ducts, soil, bottled water, and even eyewash stations [9, 31, 33, 34, 50, 55, 56, 58]. Exposure to Acanthamoeba spp. is apparently common, as 50-100% of the normal population possesses circulating antibodies specific for Acanthamoeba antigens [10, 11]. More- over, viable Acanthamoeba trophozoites can be isolated from the noses and throats of asymptomatic individuals [57]. The first case of Acanthamoeba keratitis was reported in 1973 by Jones et al. [24]. Between 1973 and 1981, only five additional cases were reported. The number of cases increased gradually from 1981 to 1984, with an increased incidence of Acan- thamoeba keratitis occurring during the late 1980s [42, 61]. Although Acanthamoeba keratitis is no longer reported to the Center for Disease Control, the general impression among clinicians is that the incidence is decreasing in North America but not in the United Kingdom. Clinical features Acanthamoeba keratitis is closely associated with contact lens wear, which appears to be the leading risk factor [40]. Over 80% of the patients diagnosed with Acan- thamoeba keratitis wear contact lenses, and soft contact lenses account for approxi- mately 75% of the cases [42]. One of the most curious features ofAcanthamoeba ker- atitis is the exquisite pain, which is not commensurate with the clinical signs. Radial neuritis or trophozoite infiltration of the corneal nerves is pathognomonic for Acan- thamoeba keratitis [41]. The severe pain and involvement of the corneal nerves by trophozoites may be related to the behavior of the trophozoites, which demonstrate a strong chemotactic response to cells of neural crest origin [54]. In vitro studies have shown that, although Acanthamoeba trophozoites kill corneal cells, they display an even greater propensity to lyse cells of neural origin [53, 54]. In addition to intense oc- ular pain, the early features of corneal infection with Acanthamoeba spp. include eye- lid-reactive ptosis, conjunctival hyperemia, and lack of discharge. Chemosis and nod- ules appear in the later stages of the disease. Corneal epithelium and sometimes the stroma are affected in the early stage of infection. As the disease progresses, stromal involvement becomes more pronounced with the development of stromal infiltrates and characteristic ring infiltrates. Other later symptoms of Acanthamoeba keratitis are the occurrence of lacuna-like changes in the ring, satellite lesions, necrotizing inflam- mation, and stromal abscess formation. Pathogenesis The pathogenesis of Acanthamoeba keratitis can follow two pathways [16, 64]. The first pathway is restricted to the epithelium without involvement of the stroma and has Immunobiologyof Acanthamoeba keratitis 149 a good prognosis. The second pathway culminates in the parasites entering the stroma, where they produce extensive necrosis and edema and provoke intense inflammation [16]. The first step in the pathogenesis of Acanthamoeba keratitis is the binding of trophozoites to the corneal epithelial surface. Animal studies have shown that binding of Acanthamoeba trophozoites to corneal epithelial cells and corneal buttons in vitro correlates with pathogenicity in vivo [20, 44, 69]. That is, Acanthamoeba trophozoites bind poorly to the corneas of animal species resistant to experimental corneal infec- tion, but adhere extensively to human, pig, and Chinese hamster corneas [44]. Acan- thamoeba trophozoites express a mannose-binding receptor, which facilitates adhesion of the parasites to mannosylated proteins on corneal epithelial cells [74]. Panjwani et al. [48] have demonstrated that free mannose strongly inhibits the binding of Acan- thamoeba trophozoites to the corneal epithelium and invasion of corneal buttons in vitro [48]. The presence of free mannose blocks parasite-mediated cytolysis of corneal cells in short-term in vitro assays [49]. However, trophozoites exposed to free man- nose 48 h or longer are induced to release one or more soluble cytolytic factors, which mediate contact-independent cytolysis of corneal epithelial cells in vitro [30]. Binding of Acanthamoeba trophozoites to either free mannose or mannosylated proteins on corneal cells promotes contact-dependent and contact-independent cytolysis of corneal cells. Pathogenic amoebae elaborate a variety of cytolytic molecules that might be elicited by engagement of the mannose receptor. Hadas and Mazur [17] examined eight species of Acanthamoeba and detected a 35-kDa serine proteinase and a 65-kDa cysteine protease. Both of these proteinases, however, are significantly smaller than the serine protease secreted by mannose-treated A. castellanii trophozoites [30]. Enta- moeba histolytica produces 5-kDa and 14-kDa protein complexes, called amoeba- pores, which form ion channels leading to the osmotic lysis of eukaryotic cells [12]. The Acanthamoeba-derived cytolytic factor induced by mannose has a molecular mass in excess of 100 kDa and is too large to be an amoebapore. In addition to killing target cells by disruption of the cell membrane, trophozoites also produce a significant amount of cell death by inducing apoptosis of the target cells [1, 53]. Following binding and erosion of the epithelial surface, trophozoites invade the deeper regions of the corneal epithelium and penetrate the stroma. Corneal invasion probably is facilitated by proteases secreted by the trophozoites [68]. A. castellanii elaborates a variety of proteases, including a 45- to 50-kDa plasminogen activator, termed Acanthamoeba plasminogen activator (aPA), which is detected in pathogenic strains of Acanthamoeba spp. but not found in non-pathogenic strains of A. castellanii [38]. It is possible, although yet to be proven, that a critical step in the pathogenic cas- cade of Acantharnoeba keratitis is the parasite's elaboration of plasminogen activator and the ensuing generation of plasmin, which in turn facilitates the parasite's invasion of the corneal epithelium and stroma. Stromal disease occurs late and is characterized by a ring infiltrate or abscess that can consist of single, multiple, or overlapping rings. The underlying cause of the ring infiltrates is unclear. Some have suggested it is the result of infiltrating neutrophils and their release of proteolytic enzymes that degrade the collagen matrix of the stroma [16]. Other investigators have proposed that the ring infiltrates are products of the
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